Maximum tag to body size ratios for an endangered coho salmon(O. kisutch) stock based on physiology and performance

Cedar M. Chittenden & Kevin G. Butterworth &

K. Fiona Cubitt & Melinda C. Jacobs &

Adrian Ladouceur & David W. Welch &

R. Scott McKinley

Received: 1 November 2007 /Accepted: 5 July 2008 / Published online: 4 September 2008# Springer Science + Business Media B.V. 2008

Abstract Many coho salmon stocks (Oncorhynchuskisutch) have been in decline during the past threedecades. Canada’s most endangered salmon stock, theThompson River coho salmon, is being studied exten-sively as managers attempt to reverse these populationdeclines. Investigators are using acoustic telemetry totrack the migratory behaviour and survival of theThompson River (and other) coho salmon stocks.Coho salmon pre-smolts are relatively small comparedwith salmonid species that are typically studied usingacoustic telemetry; therefore the identification of theappropriate sizes of fish and tags to use is critical. Thisstudy tested the effects of surgically implanting thethree smallest sizes of acoustic tags currently availableon the growth, survival, tag retention, swimmingperformance and physical condition of coho salmonpre-smolts for 300 days post-surgery. Maximum tagsize to body size ratios ranged from 15–17% by fork

length and 7–8% by mass for the three tag sizes (11 cmfork length for a 6×19 mm tag, 12.5 cm for a 7×19 mmtag, and 14 cm for a 9×21 mm tag). Based on ourresults, it is unlikely that coho salmon pre-smoltsimplanted with acoustic transmitters following thesesize guidelines would have poor survival in studies offreshwater migratory behaviour as a result of thesurgery or the tag.

Keywords Pre-smolts . Acoustic telemetry .

Tag effects

Introduction

As with many fish populations world-wide, somePacific salmon stocks have declined substantially overthe last three decades. The largest tributary to the Fra-ser River, British Columbia’s Thompson River con-tains a severely depleted population of coho salmon(Oncorhynchus kisutch; Bradford and Irvine 2000).The Thompson River coho, currently the most en-dangered salmon stock in Canada, is derived fromthe extinct Upper Columbia coho run and is geneti-cally distinct from all other coho populations in BC.Investigations into the poor status of this stock havesuggested that declining ocean productivity, freshwaterhabitat alteration, and over-fishing are likely causes(Bradford and Irvine 2000), although a complete fish-ing closure in 1998 did not improve the situation. Inan effort to pinpoint areas of high mortality for this

Environ Biol Fish (2009) 84:129–140DOI 10.1007/s10641-008-9396-9

C. M. Chittenden (*) :K. G. Butterworth :K. F. Cubitt :R. S. McKinleyThe University of British Columbia/Department ofFisheries and Oceans Centre for Aquaculture andEnvironmental Research,4160 Marine Drive,West Vancouver, BC V7V 1N6, Canadae-mail: cedar@interchange.ubc.ca

M. C. Jacobs :A. Ladouceur :D. W. WelchKintama Research Corp.,1850 Northfield Rd,Nanaimo, BC V9S 3B3, Canada

stock, researchers with the Pacific Ocean ShelfTracking (POST) project (Welch et al. 2003) haveused biotelemetry to track the riverine and early marinemigratory behaviour of free-ranging Thompson Rivercoho salmon since 2004. This research involvessurgically implanting acoustic tags into the body cavityof coho pre-smolts and subsequently tracking them inthe freshwater and marine environments. Critical tothis type of study is the understanding of what effectsthe tags and surgery may have on the survival,condition, growth and swimming performance of theanimals being monitored.

To date there are no published studies that exam-ine tag effects on coho salmon pre-smolts. Acoustictransmitters small enough to be implanted in cohosalmon pre-smolts have only been developed recently,offering a new and unique opportunity to study theearly migratory behaviour and survival of this animal.Guidelines for tag to transmitter ratios have been dis-cussed for salmonid species with larger smolts, in-cluding Atlantic salmon, Salmo salar, (Greenstreet andMorgan 1989; Moore et al. 1990; Lacroix et al. 2004);chinook salmon, Oncorhynchus tshawytscha (Adamset al. 1998a,b; Jepsen et al. 2001; Anglea et al. 2004);cutthroat trout, Salmo clarki (Zale et al. 2005) andrainbow trout/steelhead, Oncorhynchus mykiss (Lucas1989; Brown et al. 1999; Welch et al. 2007). Themaximum tag to body weight ratios discussed in thesestudies range from 2–12%, demonstrating the highvariability in sensitivity and physiology among salmonspecies (Jepsen et al. 2004). Therefore, the effects ofacoustic tags on coho salmon cannot be inferred fromstudies on other species. Given the small size of theanimals being tracked, it is critical that the effects oftransmitters on the physiology and performance of theindividuals are known. In British Columbia alone, fieldstudies using acoustic telemetry to track coho salmonmigration have been carried out in the Thompson,Nimpkish, Stamp, Keogh, Campbell and CheakamusRivers (Welch et al. 2004; Melnychuk et al. 2007;Chittenden et al. 2008). The results from this tag ef-fects study are thus important to ongoing coho salmonfield work and the Pacific-wide coho conservationeffort.

The tracking of salmon pre-smolt migratory behav-iours using acoustic telemetry has been limited by tagsize. Increasingly smaller transmitters have allowedfor the study of smaller fish; however, the limits oftag size to body size are not clear. Jepsen et al. (2002)

stated that “few studies have systematically investigat-ed the effects of different tag to body weight ratios”.The objective of our research was to determine theminimum size at which coho salmon pre-smolts couldbe implanted with three sizes of acoustic tag and sufferno effects. To meet this objective, morphological,behavioural and physiological parameters were mea-sured. A significant difference in any of these param-eters between tagged and sham or control fish wouldsuggest that the acoustic tags were having an effect onbehaviour and/or survival of tagged fish in the field.

Material and methods

Hatchery-reared Thompson River (Coldwater Creek)coho salmon pre-smolts from the Spius Creek Hatcherynear Merritt, BC, were sedated with 0.1 ppm Aquacalm(Syndel Laboratories, Vancouver, Canada) and trans-ported with supplemental oxygen to the DFO/UBCCentre for Aquaculture and Environmental Researchin West Vancouver during the springs of 2005 and2006. The fish were placed in an outdoor 244 cm-diameter fiberglass tank, supplied with aerated freshwater from Cypress Creek and fed to satiation daily.

Treatment groups

The experiments were conducted during 2005 and2006. In mid-April 2005 (1 week after transport), 224fish were divided into seven size classes ranging from9.5 to 13.0 cm fork length (Table 1). Within each sizeclass, the fish were randomly assigned to one of fourtreatment groups – control (PIT tag only), sham (surgerywithout transmitter), 6 mm tag (surgery with transmitter:6×19mm, 0.9 g in air, 0.5 g in water) and 7 mm tag (7×19 mm, 1.5 g in air, 0.8 g in water). An additional groupof fish (N=120) were reared separately for another 100days, until they were large enough (12–14 cm) to beimplanted with 9 mm tags (9×21 mm, 3.0 g in air, 2.0g in water). During this second set of surgeries, in July2005, the fish were divided into four size groups andrandomly assigned to three treatment groups (control,sham, and 9 mm tag). Following surgery these fishwere placed into the same tank as the first group. Allof the experimental fish were held in the same tank tominimize tank effects. To identify the control fish, itwas necessary to mark them with PIT tags. Theduration of this study (300 days) reflected the 9–10

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month lifespan of acoustic tags being used by manyresearchers throughout the world.

During 2006, control and 9 mm tag treatmentswere repeated with 200 fish to add larger size classes(up to 16.5 cm, Table 2) because all of the size groupstested with 9 mm tags in 2005 had low survival and tagretention. The same surgical procedures and rearingmethods were used, however no sham group was re-quired as the sham and control fish had already dem-onstrated similar growth rates during the first year ofstudy.

Surgical procedure

Prior to surgery, the fish were sedated with 0.1 ppmAquacalm and anesthetized in 60 ppm bufferedMS222 (Syndel Laboratories). They were weighed,measured and placed on the surgery table ventral sideup. The gills were gently irrigated with a maintenancedose (30 ppm) of MS222, and a wet paper towel wasplaced over the head of the fish to reduce visualstimuli. Supplemental air and Vidalife (Syndel Labo-ratories) were included in all water baths. Oxygenlevels and water temperatures were maintained toemulate source water (12.2±0.3 ppm and 6.7±0.8°Cduring the April 2005 surgical period, 9.5±0.8 ppmand 15.5±0.6°C during the July 2005 surgical period,and 10.2±0.8 ppm and 15.5±0.8°C during 2006).

PIT tags were inserted through a 2 mm incisionalong the midline of the fish, anterior to the pelvicgirdle. For the tag treatment groups, a dummy acoustictag containing a PIT tag was placed into the body

cavity through a 10 mm incision in the same location.The incision was closed with two simple interruptedsutures (absorbable Ethicon Monocryl Y513 reversecutting 4–0, 1.5 metric, 45 cm, PS-2 19 mm, 3/8 circleneedle). Sham fish underwent the same procedure astagged fish, however, only a PIT tag was inserted intothe body cavity. The Vemco dummy tags were createdto mimic the three smallest acoustic transmittersavailable, using the same coating and weight distribu-tion as regular Vemco acoustic tags. The surgical toolswere disinfected between surgeries with Ovadine(Dynamic Aqua Supply, Canada) and rinsed twicewith distilled water. All of the fish were placed in arecovery bath following surgery until normal swim-ming behaviour was resumed, whereupon they werereturned to the communal tank.

Sampling

A total of fourteen measurements of weight, forklength and healing stage were taken for the first surgerygroup (at 0, 13, 27, 41, 55, 69, 83, 95, 119, 136, 168,213, 254, and 300 days post-surgery). Similar mea-surements were taken for the second surgery group onday 0, 22, 39, 71, 116, 157, and 203 post-surgery. Thefish were anesthetized in 60 ppm bufferedMS222 priorto sampling, and were allowed to recover before beingreturned to their tank. Tag weights were subtracted fromfish weights prior to analysis. The stage of healing wascategorized as ‘poor’ (having no evidence of healing,possibly with gaps between stitches or tag protruding),‘fair’ (healing had startedwith a thin film visible over the

Table 1 Number of fish (N) in each initial fork length group by treatment for the 6 and 7 mm tag groups

9.5–10 cm 10–10.5 cm 10.5–11 cm 11–11.5 cm 11.5–12 cm 12–12.5 cm 12.5–13 cm

Control 9 10 10 10 10 – –Sham 8 10 10 10 10 11 96 mm 7 9 10 8 10 9 97 mm – – 9 9 9 8 10

Table 2 Number of fish (N) in each initial fork length group by treatment for the 9 mm tag group

12–13 cm 13–14 cm 14–15 cm 15–16 cm 16–16.5 cm

Control 16 18 24 20 8Sham 15 18 – – –9 mm 27 26 21 24 11

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incision), ‘good’ (incision mostly fused, no inflamma-tion, some stitches may remain), or ‘complete’ (incisioncompletely fused, no stitches remaining). The tank wasmonitored twice daily for expelled tags and mortalities.The percentage of tags available for detection wascalculated as: 100%×[(number of tags implanted −number of mortalities of tagged fish − numbers of tagsexpelled)/(number of tags implanted)]. During 2005, allof the fish were necropsied following termination of theexperiment, 300 days after the first surgery. Photographswere taken of each healing stage and tag position withinthe body. During 2006, all pre-smolts were euthanisedafter 90 days, weighed and measured.

Swimming performance

From 24 to 48 h after the April 2005 surgeries, theswimming performance of 40 fish from the growthand survival study was measured using proceduressimilar to Lacroix et al. (2004). Five fish from eachtreatment group (‘control’, ‘sham’, ‘6 mm tag’ and‘7 mm tag’) with fork lengths of 10.5–11 cm and fivefrom each treatment group with fork lengths of 11.5–12 cm were swum in a 4 L Blazka-style swim tube(Smit et al. 1971) for a total of ten fish per treatment.The average weight was 15.08±2.24 g (standarddeviation); the average length was 11.25±0.52 cm.Each smolt was collected from the rearing tank with adip net, placed in a bucket and transferred into thehalf-filled swim tube chamber. The chamber was thensealed and filled with water. Each pre-smolt wasgiven 20 min to acclimate at 0.1 m s−1, whereupon thespeed was increased by 0.2 m s−1. The velocity wasthen increased by 0.1 m s−1 every 10 min. The trialended when the fish rested on the back screen for 2 s.No shocks or prodding were used so as to reducestress to the fish. The fish were returned to the rearingtank following their swim trial.

During July 2005 (9 mm tag), an additional 72 fishwere prepared for the second set of swimmingperformance trials. Twenty-four fish were surgicallyimplanted with 9 mm tags; 24 fish were given shamsurgeries and 24 were controls. All pre-smolts had ini-tial fork lengths of 13.5 to 14.5 cm. The average forklength post-swim was 14.18±0.55 cm. The averagemass of the pre-smolts post-swim was 29.79±5.01 g.The fish were divided up equally by treatment group andraised indoors in four tanks. Six extra control fish wereplaced in each tank for later blood analysis [‘Control

(2005, NS)’, Table 3]. Ten of the 9 mm tagged pre-smolts expelled their tags during the 92 days leaving atotal of 14 dummy tagged fish to be swum. Thus, tokeep the three treatment groups even, a total of 42 pre-smolts were swum in the 40 L Blazka-style swim tubeusing the same methods as previously mentioned. Thelarger size of the fish tagged with 9 mm tags required alonger swim trial, necessitating a different experimentalschedule from the 6 and 7 mm tag groups. Three fishfrom the same tank (one from each treatment) wereswum per day in random order for a total of 14 swimdays, up to 90 days post-surgery (on day 1, 2, 3, 4, 5,7, 25, 27, 28, 31, 33, 34, 40 and 90). Criticalswimming speeds (Ucrits) were calculated using thefollowing formula:

Ucrit ¼ Vf þ T

t� dV

� �

where Vf is the highest velocity maintained for theprescribed time period, δV is the velocity increment, Tis the amount of time the fish swam at fatigue speedand t is the prescribed time period (Brett 1964).Following each swim trial, the fish were euthanizedin 120 ppm MS222, weighed and measured. Bloodsamples and necropsies were performed on eachindividual to compare post-exhaustive state relative tothe different treatment types. In addition to the swimtrial fish, one control (a fish that did not swim) wassampled at the end of each trial day. Blood fromuntreated fish was sampled during July 2005 and May2006 to give a baseline for comparison (‘2005 initial’,‘2006 initial’, Table 3). All experimental procedureswere approved by the Canadian Council of AnimalCare.

Blood analyses

Whole blood samples were taken from the caudalvessel of anesthetized fish with a sterile heparinizedsyringe for erythrocyte counts and analysis of hemat-ocrit (Klontz 1994). A 5 µL capillary tube was filledwith fresh blood and placed into 995 µL Hendrick’ssolution for erythrocyte counts. The remaining bloodwas centrifuged at 13,000 rpm for 5 min. Plasma wascollected and stored at -80°C until it was analysed forlevels of sodium, potassium, chloride, calcium, glu-cose and lactate using a Stat Profile Plus 9 blood gasmachine (Nova Biomedical Corporation, Massachu-

132 Environ Biol Fish (2009) 84:129–140

Table 3 Physiological measurements of coho salmon pre-smolt surgical treatment groups

Dependent variable Treatment group N Mean Standard error

Weight (g) 2005 initial (NS) 12 24.2667 1.7588Control (2005, S) 11 34.2364 1.5900Sham (2005, S) 12 28.2333 1.81309 mm tag (2005, S) 13 28.8923 2.5640Control (2005, NS) 10 26.9200 0.03202006 initial (NS) 30 16.7367 0.5292

Fork length (cm) 2005 initial (NS) 12 13.1917 0.3880Control (2005, S) 11 14.6273 0.2300Sham (2005, S) 12 14.0250 0.22009 mm tag (2005, S) 13 14.1462 0.2120Control (2005, NS) 10 13.7400 0.24202006 initial (NS) 30 11.6400 0.1230

Condition factor (g/cm3) 2005 initial (NS) 12 1.0493 0.0485Control (2005, S) 11 1.0865 0.0330Sham (2005, S) 12 1.0161 0.04709 mm tag (2005, S) 13 1.0207 0.2470Control (2005, NS) 10 1.0010 0.23702006 initial (NS) 30 1.0507 0.0116

Erythrocytes (#/mL) 2005 initial (NS) 12 1.3883 e6 5.5882 e4

Control (2005, S) 11 1.2932 e6 7.6495 e4

Sham (2005, S) 12 1.3658 e6 7.3238 e4

9 mm tag (2005, S) 13 1.1508 e6 7.0365 e4

Control (2005, NS) 10 1.2720 e6 8.0228 e4

Hematocrit 2005 initial (NS) 12 0.5477 0.0519Control (2005, S) 11 0.4258 0.0360Sham (2005, S) 12 0.4451 0.03509 mm tag (2005, S) 13 0.3880 0.0330Control (2005, NS) 10 0.3937 0.03802006 initial (NS) 24 0.4675 0.0137

Mean cell volume (nm3) 2005 initial (NS) 11 3.3247 e−4 0.0000Control (2005, S) 14 3.2084 e−4 0.0000Sham (2005, S) 13 4.1697 e−4 0.00009 mm tag (2005, S) 13 3.1432 e−4 0.0000Control (2005, NS) 12 3.7125 e−4 0.0000

Sodium, plasma (mmol/L) 2005 initial (NS) 10 207.9600 2.7237Control (2005, S) 11 241.6727 10.7290Sham (2005, S) 12 236.4000 10.27209 mm tag (2005, S) 13 239.9077 9.8690Control (2005, NS) 10 233.8800 11.2530

Potassium, plasma (mmol/L) 2005 initial (NS) 10 4.0880 0.4378Control (2005, S) 11 8.3091 1.0330Sham (2005, S) 12 11.6667 0.98909 mm tag (2005, S) 13 7.1354 0.9500Control (2005, NS) 10 9.9640 1.08402006 initial (NS) 26 5.7651 0.5544

Cloride, plasma (mmol/L) 2005 initial (NS) 10 176.9200 3.0264Control (2005, S) 11 171.6727 4.6260Sham (2005, S) 12 170.5667 4.42909 mm tag (2005, S) 13 175.3231 4.2560Control (2005, NS) 10 174.4800 4.85202006 initial (NS) 26 146.7532 3.9209

Calcium, plasma (mmol/L) 2005 initial (NS) 10 1.8280 0.0253

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setts). Cortisol was measured using a cortisol Elisa kitfrom Immuno Biological Laboratories America, Inc.(Minneapolis, MN, USA). Condition factors werecalculated as mass × fork length−3 (Goede and Barton1990). Erythrocyte counts were determined manuallywith a microscope and hemacytometer.

Statistical analyses

The size data were found to be normally distributed(normal scores>0.2 using Kolmogorov–Smirnov)with equal variance (F76, 3,410=31.927–54.67, p<0.0001). General linear models (GLM) were devel-oped for each initial size group (Tables 1, 2 and 3)with days since surgery and treatment as fixed factors,and weight, fork length and healing as dependentvariables. GLMs were also created for swimmingperformance data and blood data. Multivariate anal-yses and Scheffe’s post-hoc method were used toanalyse differences between treatments, as N valuesvaried between treatments and sample days. Percentdata (hematocrits) were arcsine transformed prior tostatistical analysis. In all cases, significance was estab-lished at p<0.05.

Results

For each tag type, we examined growth, healing rates,survival, tag retention, swimming performance andphysical condition for up to 300 days post-surgery.All control and sham groups had 88% survival orhigher until the termination of the study.

Growth

For the smallest tag (6 mm diameter), there was asignificant difference in body size (weight and length)among the three treatments in the 9.5–10 cm groupuntil 140 days post-surgery. Similarly, in the 10–10.5 cmand 10.5–11 cm groups, there was a significantdifference between the tagged and control/sham fish inbody size until 140 days post-surgery; however therewas no observable difference between the sham andcontrol groups (Fig. 1a). For the three previouslymentioned size groups, there was no size differenceamong treatment groups after 140 days post-surgery.The 10.5–11 cm group tagged with 7 mm diametertransmitters had significant differences between thecontrol/sham groups and the tagged group in length

Table 3 (continued)

Dependent variable Treatment group N Mean Standard error

Control (2005, S) 11 1.6218 0.0390Sham (2005, S) 12 1.4300 0.03709 mm tag (2005, S) 13 1.6431 0.0350Control (2005, NS) 10 1.5120 0.04002006 initial (NS) 26 1.1873 0.0331

Glucose, plasma (mmol/L) 2005 initial (NS) 10 6.0000 0.5750Control (2005, S) 11 8.1455 0.5700Sham (2005, S) 12 8.3333 0.54609 mm tag (2005, S) 13 8.1231 0.5240Control (2005, NS) 10 7.3600 0.59802006 initial (NS) 26 6.0780 0.3231

Lactate, plasma (mmol/L) 2005 initial (NS) 10 6.6000 0.4511Control (2005, S) 11 6.9455 0.7290Sham (2005, S) 12 5.9333 0.69809 mm tag (2005, S) 13 7.8154 0.6710Control (2005, NS) 10 4.7600 0.76502006 initial (NS) 25 7.6220 0.5171

Cortisol, plasma (mmol/L) 2005 initial (NS) 5 35.8605 13.7980Control (2005, S) 11 94.5211 32.4660Sham (2005, S) 12 70.2966 31.08409 mm tag (2005, S) 13 84.3371 29.8640Control (2005, NS) 10 92.7771 34.0510

Pre-smolts sampled after the completion of a swim trial were labeled with an ‘S’; those that did not swim were labeled ‘NS’

134 Environ Biol Fish (2009) 84:129–140

(data not shown) but not weight (Fig. 2a). There was nosignificant size difference among treatments above aninitial fork length of 11 cm for fish implanted witheither the 6 or 7 mm tag (Figs. 1b and 2b).

Survival and tag retention were low in the 9 mm tagtreatment group when the initial fork length was < 13 cm,which left too few fish to compare size statistically. Thesize groups were therefore pooled into 1 cm size groupsto get large enough numbers for a statistical analysis.There was no significant difference in size betweentagged and control/sham fish above an initial fork lengthof 14 cm.

Healing rates

The controls in all size groups of the first set ofsurgeries had a ‘good’ healing status 2.5 months post-surgery, and were all completely healed 3 monthspost-surgery. The sham groups showed greater variancein healing time; 90% of individuals reached a ‘good’status between 2.5 and 3months, and a ‘complete’ statusbetween 3 and 5 months. Eighty percent of fish taggedwith 6 and 7 mm tags had a ‘good’ status by threemonths and were completely healed at 7 months post-

surgery. Healing improved slightly as initial size atsurgery increased.

For the second group of surgeries (larger fish,9 mm tag), the control fish reached a ‘good’ healingstatus by the first sampling 22 days post-surgery, andwere completely healed by day 71. The sham fish hada ‘good’ healing status between day 39 and 116,however they never reached ‘complete’. In the largestsize group (13–14 cm) tagged with large tags in thefirst year’s study a few survivors had a ‘good’ statusat day 116. During the second year, the majority ofpre-smolts of initial fork length 14–16.5 cm taggedwith large tags were completely healed by 90 dayspost-surgery. Necropsies of the experimental fishshowed that some tags were adhering to the bodycavity wall, fat tissue or organs. Some tags weresurrounded by tissue and expelled through theincision site.

Survival and tag retention

We observed 100% survival and tag retention in allsize groups of fish tagged with 6 mm tags up to50 days post-surgery. There were two mortalities in

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Fig. 1 Weight over time for the 6 mm tag group of initial forklength a 10.5–11 cm and b 11–11.5 cm. The control group isdefined by a dashed line, the sham group a dotted line and thetagged group a solid line. Standard error bars are included for all

three. In the 10.5–11 cm group, note the significant differencebetween tagged and control/sham weight up to 140 days post-surgery. There were no significant differences between treatmentgroups for fish with initial fork lengths over 11 cm

Environ Biol Fish (2009) 84:129–140 135

the smallest size group 75 and 78 days post-surgery,and some tag loss in three of the size groups (Table 4,6 mm tag group). Above initial fork lengths of 10 cm,survival was 100% and tag retention was over 88%until the termination of the experiment, 300 dayspost-surgery. For the 7 mm tag group there was 100%survival in four out of five of the tagged groups, how-ever there was some tag loss in pre-smolts up to aninitial fork length of 12.5 cm (Table 4, 7 mm taggroup). All control fish and over 90% of the sham fishsurvived until the end of the study.

The 9 mm tag was too large to fit in the body cavityof the smallest size group (12–13 cm) and as a result,many fish had to be euthanized during surgery. Of thosethat did survive, the majority expelled their tags veryquickly and few lived until the end of the experiment(Table 4, 9 mm tag group). Above initial fork lengthsof 14 cm, there was 100% survival to day 50 post-surgery; however tag retention began to fall after threeweeks. By three months, there were only 42% of thetags remaining in fish up to 16 cm. Above 16 cm therewas 55% tag retention (Table 4, 9 mm tag group).

Swimming performance

There were no significant differences in Ucrit orvariance between treatment groups in either m∙s−1 or

bl s−1 (Table 5). Pre-smolts that were included in theswim trials had no difference in survival, tag retention,healing or growth when compared with pre-smolts thatwere not included in the swim trials. There was nodifference in swimming performance between rearingtanks.

Blood analyses

Plasma levels of calcium were lower in sham groupsthan in control and tag groups (Table 3). No othersignificant differences were found in blood analysesbetween swum groups. Initial levels of plasma sodium,potassium, chloride, glucose and cortisol were allsignificantly lower than levels observed in swum fish.

Discussion

Acoustic telemetry has proven to be a very usefulmethod to track the early marine migratory behaviourand survival of fish species, including salmon pre-smolts(Welch et al. 2003). With the development of 6 and7 mm diameter acoustic tags, the pre-smolts of smallersalmonids such as coho, are now able to be tracked. Weconducted this study to determine the maximum tag to

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tagged group a solid line. Standard error bars are included forall three. There were no significant differences in weight amongtreatment groups in either group

136 Environ Biol Fish (2009) 84:129–140

body size ratios at which coho pre-smolts would sufferno adverse effects on survival, growth, physiology andswimming performance.

Further investigations could be made into the tags’effects on the buoyancy, startle response, disease

resistance, and foraging ability of coho salmon pre-smolts. Laboratory environments can not replicateconditions that the tagged fish might encounter in thewild. Therefore, while we are able to find tag to bodysize ratios at which the survival, growth, swimming

Table 5 Critical swimming speeds of control, sham and tag groups

Treatment group N Mean Standard error

Ucrit (m s−1) Control (6, 7 mm) 10 0.3531 0.0260Sham (6, 7 mm) 10 0.4436 0.02606 mm tag 10 0.3705 0.02607 mm tag 10 0.3470 0.0260Control (9 mm) 13 0.9963 0.0630Sham (9 mm) 13 1.0548 0.06009 mm tag 13 1.0908 0.0600

Ucrit (bl s−1) Control (6, 7 mm) 10 3.1558 0.2340

Sham (6, 7 mm) 10 3.9390 0.23406 mm tag 10 3.3076 0.23407 mm tag 10 3.0718 0.2340Control (9 mm) 13 6.8218 0.4310Sham (9 mm) 13 7.5346 0.41409 mm tag 13 7.7811 0.4140

Table 4 Percent survival and tags available for detection over time in the 6 mm tag group, 7 mm tag group and 9 mm tag group

Days since surgery % Surv % Tags % Surv % Tags % Surv % Tags % Surv % Tags % Surv % Tags

6 mm tag groupInitial size group 9.5–10 cm 10–10.5 cm 10.5–11 cm 11–11.5 cm 11.5–12 cm50 100 100 100 100 100 100 100 100 100 100100 72 43 100 89 100 100 100 88 100 100300 72 43 100 89 100 100 100 88 100 100

7 mm tag groupInitial Size Group 10.5–11 cm 11–11.5 cm 11.5–12 cm 12–12.5 cm 12.5–13 cm7 100 100 100 100 100 100 100 100 100 10014 100 100 100 89 100 100 100 100 100 10035 100 78 100 89 100 100 100 100 100 10042 100 67 100 89 100 100 100 100 100 10050 100 55 100 78 100 89 100 75 100 100100 100 55 100 78 100 89 89 50 100 100300 100 55 100 78 100 67 89 50 100 100

9 mm tag groupInitial size group 12–13 cm 13–14 cm 14–15 cm 15–16 cm 16–16.5 cm1 100 59 100 100 100 100 100 100 100 1007 48 48 92 92 100 100 100 100 100 10021 48 41 92 92 100 100 100 100 100 10028 48 26 92 88 100 81 100 88 100 9135 48 18 92 81 100 67 100 67 100 7350 48 15 92 62 100 52 100 46 100 6490 48 7 92 54 95 43 100 42 100 55200 48 4 92 35 – – – – – –

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performance and physiology of coho pre-smolts was notsignificantly affected in an artificial environment, theremay be affected behaviours in the field, such as foragingor predator avoidance ability.

Surgically implanted tags that were up to 8% of thefish’s mass and up to 17% of their fork length had nosignificant effect on the survival, growth, swimmingperformance, or physical condition of ThompsonRiver coho salmon pre-smolts. Swimming perfor-mance trials conducted on 5–10 g rainbow troutimplanted with acoustic tags demonstrated no observ-able effect from tags that were 6–12% of the fish’sweight (Brown et al. 1999), which contradictedWinter’s controversial ‘2% rule’ (1983). Predatoravoidance and swimming performance in juvenilechinook were not significantly affected by implantedtags that were 6.7% of the fish’s body mass (Angleaet al. 2004). Adams et al. (1998b) found that radiotags implanted in chinook up to 12 cm lowered theircritical swimming speeds; a lower 2.2–5.6% tag tobody mass ratio was recommended. Cutthroat troutimplanted with tags that were 4% of their bodyweight had only slight decreases in growth andperformance (Zale et al. 2005). Thompson River cohosalmon pre-smolts had no difference in swimmingperformance 24 to 48 h post-surgery for fish 10.5–12cm long implanted with 6×19 mm (6% by weight,17% by length) and 7×19 mm tags (10% by weight,17% by length). The Ucrit values we measured (Table5) were similar to those observed for coho smolts(3.5–5.5 bl s−1) by Glova and McInerney (1977).Coho salmon pre-smolts with fork lengths of 13.5–14.5 cm implanted with 9×21 mm tags had similarUcrits to sham and control fish (the tags were 10% oftheir weight in air and 7% of their fork length).

The condition factors of the Coldwater River cohosalmon pre-smolts were >1.0 g cm−3 on average,which resembled other hatchery-reared coho popula-tions but was likely greater than their wild-rearedcounterparts (Chittenden et al. 2008). Plasma levels ofsodium and chloride were higher than normal in allgroups (Wedemeyer et al. 1990), suggesting apossible bias due to measurement or storage time.Potassium was high for swum fish only (Wedemeyeret al. 1990). Plasma concentrations of sodium, chlorideand potassium ions have been found to increase withexercise and stress levels in fresh water, which couldexplain differences found between swum and non-swum fish (Graham et al. 1982). Erythrocyte counts,

hematocrits, mean cell volumes, calcium, glucose,lactate and cortisol levels were within normal rangesfor coho pre-smolts (Wedemeyer et al. 1990).

Previous work examining the effects of tag insertioninto salmonids has shown substantial variation be-tween species in terms of growth, survival and tagretention. In their research on Atlantic salmon, Lacroixet al. (2004) compared the effects of three lengths of8 mm diameter tags. They recommended using fishwith a tag to fork length ratio of 16% or less, and atag to fish mass ratio of 8% or less. With the tags theyused, this corresponds to fish that were 14–15 cm longor 35–45 g. This study, carried out on coho salmonpre-smolts between 9.5 and 16.5 cm long, found nodifferences in growth between tag, control and shamgroups above fork lengths of 11 cm for 6 mm and7 mm-diameter surgically implanted acoustic tags andabove 14 cm for 9 mm-diameter tags. All coho salmonpre-smolts implanted with 6 mm tags had excellentsurvival and tag retention above fork lengths of 10 cm;the same results were found in pre-smolts over 12.5 cmfor the 7 mm tag. Rainbow trout/steelhead were foundto have reduced growth to day 21 for 11.4–15.9 cm fish(Lucas 1989) and less than 15% tag loss to day 84 infish over 14 cm tagged with 8×24 mm acoustic tags(Welch et al. 2007). The coho salmon pre-smolts im-planted with 9×21 mm tags had excellent survivalabove initial fork lengths of 14 cm; however tag re-tention in pre-smolts up to 16.5 cm dropped from 81–91% after one month to 42–55% after three months.These results are of major importance to long-termfield studies that estimate survival of coho salmonpre-smolts implanted with 9 mm transmitters. Forshorter-term telemetry studies, smaller fish could betagged to cover more of the population curve, as long-term survival, growth and tag retention may not be asimportant. However, the swimming ability and be-haviour of the smaller fish could be more affectedthan that of the larger fish.

This study examined the effects of three sizes ofimplanted acoustic tags on the long-term growth,healing, survival, tag retention, swimming performanceand physical condition of endangered Thompson Rivercoho salmon pre-smolts. We recommend that coho begreater than 11 cm (17% tag to fork length ratio) or15 g (7% tag to body mass ratio) for implantation witha 6×19 mm tag (0.9 g in air, 0.5 g in water). Although11 cm fish tagged with a 7×19 mm tag (1.5 g in air,0.8 g in water) grew at similar rates to control groups,

138 Environ Biol Fish (2009) 84:129–140

when survival and tag retention are taken into consid-eration, a minimum of 12.5 cm is more appropriate(15% tag to fork length ratio or 7% tag to body massratio). If a 9×21 mm tag (3.0 g in air, 2.0 g in water) isbeing used, pre-smolts over 14 cm (15% tag to forklength ratio), or 35 g (8% tag to body mass ratio) arerecommended, however tag retention levels droppedsignificantly after 1 month.

Acknowledgements Thanks to N. Richardson, S. Dean, J.VanVuuren, J. Shiller, and L. Skinner for their help withsampling and feeding, to K. Hunter, S. Balfry and C. Biagi fortheir assistance and advice, and to the two anonymousreviewers for their helpful comments on the manuscript.Thanks to the fish used in this experiment, the Spius CreekHatchery staff and the National Science and EngineeringResearch Council of Canada.

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